Significance of Concealed Feeding Habits in the Evolution of
Sawflies of the Subfamily Nematinae (Hymenoptera, Tenthredinidae)

A. G. Zinovjev

Tenthredinidae (Hymenoptera, Symphyta) are the largest family of
plant-feeding Hymenoptera. Larvae usually feed externally on
plants, although there are quite a few endophytic species (for instance,
all Fenusini and Heterarthrini are typical miners.) The subfamily Nematinae, which constitutes one of the most
distinct and advanced groups in the family, includes many species
with concealed feeding habits.

Nematinae are strikingly different from the rest of
Tenthredinidae in reduction of the number of prolegs, which present on
abdominal segments 2-7 and 10 rather than 2-8 and 10 (although
similar reduction is found in some Fenusini). It is only in the
nematine larvae that we find median ventral eversible glands. In
the free-living species, these protruding odorous appendages are
believed to play a repellent role. Glands of this kind in the
gall-making Pontania as well as other endophytic nematine
groups have been considered as evidence of the origin of these
groups from some free-living ancestors (Smith 1970). However,
the fact that endophytic groups possess ventral glands can hardly
be considered proof of their descent from free-living ancestors,
since it is hardly possible that the current function of defense
had been their original function. On the contrary, it is far
more possible that the free-living forms originated from those
with a concealed feeding habit. The purpose of this article is to
justify this assumption.

The reduction of antennal segments is an important diagnostic
character of nematine larvae and may serve well as evidence in
favor of this hypothesis. In the entire family, this kind of
reduction is typical only in highly specialized miners, such as
Fenusini, Heterarthrus, as well as Nematinae,
including their concealed as well as free-living members. This
fact can be anything but an accidental phenomenon. The rest of
the Tenthredinidae larvae have very distinct conical five-segmented
antennae. Within the Nematinae, only Hemichroa
larvae are known to have five-segmented antennae (Lorenz & Kraus
1957). The majority of Nematinae have four- and even three-segmented
short antennae that hardly or not at all project above
the surface of the head capsule (Fig. 12, 13).

Of all the Nematinae, it is only in a few free-living species
that the most developed antennae are found. As for the endophytic
Nematinae, fully developed antennae are found only in the most
primitive group, Hoplocampa. One can attribute the
distinct reduction of the antennae to the advanced evolutionary
status of the group as well as to the endophytic habit of larvae.
The reduction of the antennae is particularly typical for such
highly advanced and, at the same time, endophytic groups as
Pontania and Euura. On the other hand, similar,
completely flat antennae are also found in some larvae with free-living
habits in advanced as well as primitive Nematinae
(Fig. 13). This could be attributed to the fact that the
endophytic habit was common in ancestors of the more recent
groups.

Another distinctive feature of many nematine larvae is the
presence of a pair of 'caudal protuberances', the so-called
cerci or, to be more precise, pseudocerci. Although they
constitute protrusions at the posterior margin of the last
tergite, they are not homologous to the cerci of adults, nor to
ones of other insects (Middleton 1921). Both the shape and
position of the pseudocerci in Nematinae are greatly variable.
In the free-living Hemichroa larvae, the entire margin of
the anal tergite is armed with multiple short denticles; other
Nematinae may have only a single pair of pseudocerci.

Pseudocerci may be positioned laterally, as in Phyllocolpa (Fig. 10)
and some Pontania with concealed feeding habits as well as
in free-living Croesus,Nematus, and many
Amauronematus. In some free-living species, the lateral
pseudocerci are fully developed and swollen at their apices; in
others, they may be nearly completely reduced.

Until recently, medially positioned pseudocerci have been known exclusively in
endophytic groups, such as Caulocampusacericaulis
(MacGillivray) (a miner in maple leaf petioles) as well as some
gall-making Pontania. In both groups, the last tergite is
attenuated into the medial caudal protrusion bearing small medial
pseudocerci at its apex (Fig. 8, 9); in Caulocampus, the
attenuation is chitinized (Yuasa 1922).

Typical medial pseudocerci recently have been found among
free-living nematine larvae belonging to the subgenus Nematus
(Paranematus) (Vikberg 1972, Zinovjev 1978). In Paranematus
the development of the caudal protrusions may be highly variable in
different species as well as different specimens of the same
species. The pseudocerci tend to become shorter with age
of larvae; in the last instars pseudocerci are shortened or
even reduced to inconspicuous tubercles in some specimens
(Fig. 3, 4, 5).

Caudal appendages are known in many different insects; however,
they are most characteristic of those with concealed feeding
habits. These appendages may be used for excavation (similarly
to those of the Ipidae), or be organs of support and locomotion,
or else sensors. Sensor appendages are often found laterally,
as, for example, those of Pamphiliidae and Megalodontidae larvae,
which live in webbed nests or leaf curls. In case the support
function dominates, the medial location appears to be most
efficient. The extreme example is probably the single supra-anal
thorn (or cornus), which is found in Siricidae, Xiphydriidae, and Cephidae larvae
(Fig. 1). Appendages that are considered to be organs of support
are known in many other insects: cremasters in mobile Noctuidae pupae,
urogomphi in Elateridae larvae,
similar appendages in Tenebrionidae and Xylophagidae (Fig. 2),
and others (Gilyarov 1949, Gilyarov 1964, Krivosheina 1969, and others).
In Tenthredinidae, some species of Fenusa appear to have an analogous
organ, a single denticle (Fig. 6, 7). Apparently, its development may
be attributed to the mining habit of Fenusini as well as to the
reduction of the last pair of prolegs.

The medial pseudocerci of Caulocampus and Pontania,
as mentioned by Yuasa (1922), most probably have the same
function as the supra-anal thorn of Siricidae. There is striking
similarity between the pseudocerci (the lateral as well as
medial) of nematine larvae and support appendages of a vast
variety of insects with concealed feeding habits (Fig. 3-10).
This resemblance may be interpreted as evidence of correlation
between the development of this kind of organs and the concealed
feeding habit. The wide occurrence of pseudocerci among free-feeding
larvae might point to their origin from endophytic
ancestors.

It is worth mentioning that the dorsal swellings in the larvae of
Pontopristia amentorum (Foerster) (which live in
willow catkins) also have been considered to be organs of locomotion
(Conde 1938). Although these swellings are very well developed
in Pontopristia larvae, they are as well present in many
free-living groups.

All these facts thus support the hypothesis that the concealed
feeding habit (either mining or close to mining) was
characteristic of Nematinae larvae as long ago as during the
earliest stages of their evolution. Among the extant Nematinae,
Pseudodineurini (Pseudodineura,Endophytes, and
Kerita) are typical leaf miners; an archaic Nearctic
species, Caulocampus acericaulis, is a petiole
miner. Species of Hoplocampa, the most primitive of the
subfamily, bore in fruits of Rosaceae.

Gall-making appears to be a more specialized habit that occurs in
advanced Nematinae (Pontania and Euura).
Pachynematuspumilio Konow
[now Bacconematuspumilio] appears to belong to
this ecologic group as well. It inhabits black currant berries
inducing abnormal, distorted growth.

A number of Nematinae demonstrate a kind of transitional habit
between concealed and free-living ones. Here belong all of
Phyllocolpa and also Micronematusmonogyniae
(Hartig), which produce leaf folds. One may add here
Sharliphoraambigua (Fallen), which builds a
shelter of young spruce needles connecting them with the
excretion of its silk glands, as well as the species of
Pontopristia, which live in willow catkins.
[Apparently, larvae with transitional habits differ from the free-living ones
in their humidity requirements.]
Even among the free-feeders, humidity requirements
may be quite variable, for example, if one compares those living on upper and lower
surface of the leaf blade (Benson 1950).

Some Nematinae species change their habit in the process of larva
development. In Pristiphora angulata Lindqvist,
the first-instar larvae feed inside Spiraea flower buds,
and later instars come out onto the surface of the opening buds
or even on the leaves. In this case, the endophytic stage might
be non-obligatory.

Among the free-living Amauronematus, there are species
that are concealed at the initial stages of development. These
are A.viduatus (Zetterstedt) probably together with some
other closely related species, which are sometimes segregated into
a separate genus Decanematus in accordance with peculiar structure of
their ovipositor. The last-instar larvae of
A.viduatus have been found feeding free on the
leaf surface, whereas their earlier instars usually live
concealed inside crowded, distorted upper leaves of young willow
shoots. This kind of 'gall', looking much like the damage made by a
tortricid, is formed as young leaves lose their ability to grow
apart from each other.

There is also evidence that habit changes take place in some
Phyllocolpa. The larvae of Ph.purpureae
(Cameron) live inside rolled leaves of Salix
purpurea and feed on the leaf tissue leaving the upper
cuticle intact. On opening an infected leaf at the early stages,
one notices an underdeveloped mine with a few excrements and a
round hole, through which the larva has exited. All that is left
inside the mine is the lower cuticle and a layer of deformed
upper parenchyma. When opening leaf rolls at later stages, one
no longer can see a conspicuous mine, as the stretched lower
cuticle breaks promptly. The upper layer of deformed tissue at
the place of oviposition resembles a somewhat underdeveloped
Pontania gall and can be recognized even on old leaves.

Phyllocolpapiliserra (Thomson), an inhabitant of
rolled leaves of Salixviminalis and
S.dasyclados, presents a very different case of
habit change. A gregarious feeding habit is typical for the
larvae; one may find 6-7 of them together in one leaf roll.
Naturally, one leaf cannot provide enough food for all larvae;
therefore, at the last instar, they feed freely on the adjacent
leaves and use their leaf roll as a shelter during the daytime.

The Phyllocolpa species mentioned above are two extreme
examples. Other Phyllocolpa habits may be placed easily
between these two. In some species, such as Ph. anglica
(Cameron), larvae feed inside the leaf roll during all the
instars. In others, like Ph.leucapsis
(Tischbein), late instars feed at the leaf margin right near the
fold; however, they do not appear to leave their shelter
completely while feeding. Yet another way of feeding is seen in
Ph.leucosticta (Hartig). Last instars of this
species appear to make holes at random on the entire leaf surface
(as opposed to Ph.leucapsis and other closely
related species that feed at the leaf margins). For that
purpose, the larva has to temporarily leave its leaf fold, at
least when it is feeding on large leaves of Salixcaprea. These habits culminate with
Ph.piliserra mentioned above, which feeds almost
freely during its last instar. Species of the closely related
genus Nematus that live free during all instars may be
considered as a natural extension of this series. The existence
of transitional forms may be explained easily if the concealed
feeding habit is considered to be primary. It is much more
difficult to imagine the opposite way of the evolution.

One of the adaptations of the free-living Nematinae to the water
deficit is their cryptonephridial system that has the function of
water absorption from the rectum. Only Caulocampus larvae
lack the the cryptonephridial system. In this genus, Malpighian
tubules are the most primitive. They are loosely positioned, not
attached to the intestine (Maxwell 1955). As for all the other
species, terminal parts of their Malpighian tubules form a more
or less dense, convoluted layer over the surface of the rectum.
This facilitates absorbing water from the excrements. Besides,
the number of Malpighian tubules has a tendency to increase,
which can be easily traced within the subfamily. This fact may
be as well attributed to the necessity of saving water in
connection with the free-living habit. The smallest number of
Malpighian tubes (6-12) is found in Caulocampus,Hoplocampa,Kerita,Pontania, and
Euura (Maxwell 1955), all of which have a concealed living
habit. In the free-living larvae, the number of Malpighian tubes
is as high as 20 to 38 (usually about 28). An intermediate number
of Malpighian tubes (14-16) is known only for three species:
Priophorus sp., Anoplonyx sp. (Maxwell 1955), and
Stauronematuscompressicornis (F.) (the latter has
about 16, orig. data). These facts as well fit the proposed
evolutionary outline of habits in Nematinae. However, they
cannot be considered as evidence in favor of the assumption that the concealed feeding habit
is the most primitive. One cannot exclude a possibility of a
secondary reduction of the Malpighian tubes in case the opposite
change from the free to concealed habit has occurred (Maxwell
1955).

As shown by Gilyarov (1949), the concealed habit was
ancestral in all the large groups of Holometabola. Ancestors of
Symphyta, that is, of all Hymenoptera might have had a more or
less concealed habit (Gilyarov 1929, Rasnitsyn 1969). However,
problems concerning the evolution of all sawflies are beyond the
scope of this article. I would just mention here that the
reduction of the antennae is characteristic of not only
Nematinae, but also other Tenthredinoidea, such as
Diprionidae, Cimbicidae, and Argidae. Among Tenthredinoidea,
it is only in the free-living Tenthredinidae and the archaic
Blasticotomidae that fully-developed antennae are found. Mining
species beside Nematinae are known in Argidae. Some of the
free-living Argidae also have pseudocerci.

So far, the free-living habit has been considered to be primary for
Tenthredinidae larvae. The presence of prolegs on their abdominal segments
has been emphasized in support of this hypothesis.
If we accepted that free feeding was primary in all Tenthredinidae and, at the
same time, that the concealed habit was primary in Nematinae, then
we could conclude that both the free feeding and concealed habit
of Nematinae larvae were to be considered secondary within
Symphyta. However, the assumption of an evolutuionary inversion,
like this, is not sufficiently justified [since we cannot state
for sure that the free-living habit was characteristic of the
ancestors of Tenthredinidae.]

As a matter of fact, locomotory appendages on the abdominal
segments are characteristic of concealed forms as well as free-living ones.
In Holometabola larvae, one can trace the
development of prolegs and similar appendages many times in
different groups. In a number of cases, this development is
correlated with the concealed habit rather than free-living
habit. One may, therefore, speculate that prolegs had appeared in
Symphyta at least earlier than Symphyta completed their
transition to the free-living habit and, besides, independently
in different groups. In this connection, of particular interest
is the fact that many comparatively primitive groups of
Tenthredinidae (almost all Dolerini, Selandria of the
Selandriini) feed on plants with fistular stems such as horsetails
(Equisetum), rushes (Juncus), or grasses. Among
the species of Dolerus, there are some that hide inside
horsetail stems during the daytime (Lorenz and Kraus 1957).

As for the free-living nematine larvae, not only may we imagine
their evolution from some endophytic forms, but also assume that
this happened several times, independently, in different groups
of the subfamily. Widespread occurrence of the endophytic habit
as well as different types of transitional habits among the
Nematinae may be considered alone as an indication of this kind
of parallel evolution. The development of the cryptonephridial
system in Nematinae might have been a prerequisite for their
transition to free living, since dehydratation appears to be the
most critical factor in connection with the shift toward the
free-living habit.

Zinovjev, A. G. 1978. Description of a new subgenus Paranematus
subgen. n. for the group of species related to Nematus wahlbergi Thomson
(Hymenoptera, Tenthredinidae) with a review of species from
the European part of the USSR. Entomol. obozr. 57: 625-635.
(in Russian, with English summary.)